Defence priming in tomato by the green leaf volatile (Z)-3-hexenol reduces whitefly transmission of a plant virus.

Green leaf volatiles (GLVs) can induce defence priming, that is, can enable plants to respond faster or more strongly to future stress. The effects of priming by GLVs on defence against insect herbivores and pathogens have been investigated, but little is known about the potential of GLVs to prime crops against virus transmission by vector insects. Here, we tested the hypothesis that exposure to the GLV Z-3-hexenol (Z-3-HOL) can prime tomato (Solanum lycopersicum) for an enhanced defence against subsequent Tomato yellow leaf curl virus (TYLCV) transmission by the whitefly Bemisia tabaci. Bioassays showed that Z-3-HOL priming reduced subsequent plant susceptibility to TYLCV transmission by whiteflies. Z-3-HOL treatment increased transcripts of jasmonic acid (JA) biosynthetic genes and increased whitefly-induced transcripts of salicylic acid (SA) biosynthetic genes in plants. Using chemical inducers, transgenics and mutants, we demonstrated that induction of JA reduced whitefly settling and successful whitefly inoculation, while induction of SA reduced TYLCV transmission by whiteflies. Defence gene transcripts and flavonoid levels were enhanced when whiteflies fed on Z-3-HOL-treated plants. Moreover, Z-3-HOL treatment reduced the negative impact of whitefly infestation on tomato growth. These findings suggest that Z-3-HOL priming may be a valuable tool for improving management of insect-transmitted plant viruses.